Regulation of cnidarian–dinoflagellate mutualisms: Evidence that activation of a host TGFβ innate immune pathway promotes tolerance of the symbiont

Developmental and Comparative Immunology

Volumn 38, Issue 4, 2012, Pages 525-537

  Detournay, Olivier ^a   Schnitzler, Christine E ^a   Poole, Angela ^a   Weis, Virginia M ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

Aiptasia; Cnidarian; Coral bleaching; Dinoflagellate; Innate immunity; Nematostella; Smads; Symbiodinium; Symbiosis; Transforming growth factor beta

Indexed keywords

LIPOPOLYSACCHARIDE; NITRIC OXIDE; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; DINOFLAGELLATE; GENETICS; HEAT SHOCK RESPONSE; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; SEA ANEMONE; SIGNAL TRANSDUCTION; STATISTICAL MODEL; SYMBIOSIS;

AMINO ACID SEQUENCE; ANIMALS; BAYES THEOREM; CONSERVED SEQUENCE; DINOFLAGELLIDA; HEAT-SHOCK RESPONSE; IMMUNITY, INNATE; LIKELIHOOD FUNCTIONS; LIPOPOLYSACCHARIDES; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; NITRIC OXIDE; PHYLOGENY; SEA ANEMONES; SIGNAL TRANSDUCTION; SMAD PROTEINS; SYMBIOSIS; TRANSFORMING GROWTH FACTOR BETA;

MLCS; MLOWN;

EID: 85027959032     PISSN: 0145305X     EISSN: 18790089     Source Type: Journal    
DOI: 10.1016/j.dci.2012.08.008     Document Type: Article

References (73)

1. Abascal, F., Zardoya, R., Posada, D., ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21 (2005), 2104–2105.
2. Adl, S.M., Simpson, A.G.B., Farmer, M.A., Andersen, R.A., Anderson, O.R., Barta, J.R., Bowser, S.S., Brugerolle, G.U.Y., Fensome, R.A., Fredericq, S.Y.T., Karpov, J.S., Kugrens, P., Krug, J., Lane, C.E., Lewis, L.A., Lodge, J., Lynn, D.H., Mann, D.G., Mccourt, R.M., Mendoza, L., Moestrup, Ø., Mozley-Standridge, S.E., Nerad, T.A., Shearer, C.A., Smirnov, A.V., Spiegel, F.W., Taylor, M.F.J.R., The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Euk. Microbiol. 52 (2005), 399–451.
3. Belladonna, M.L., Volpi, C., Bianchi, R., Vacca, C., Orabona, C., Pallotta, M.T., Boon, L., Gizzi, S., Fioretti, M.C., Grohmann, U., Puccetti, P., Cutting edge: autocrine TGF-beta sustains default tolerogenesis by IDO-competent dendritic cells. J. Immunol. 181 (2008), 5194–5198.
4. Bogdan, C., Nathan, C., Modulation of macrophage function by transforming growth factor beta, interleukin-4, and interleukin-10. Ann. N Y Acad. Sci. 685 (1993), 713–739.
5. Clark, R.I., Woodcock, K.J., Geissmann, F., Trouillet, C., Dionne, M.S., Multiple TGF-beta superfamily signals modulate the adult Drosophila immune response. Curr. Biol. 21 (2011), 1672–1677.
6. Colley, N.J., Trench, R.K., Cellular events in the reestablishment of a symbiosis between a marine dinoflagellate and a coelenterate. Cell Tissue Res. 239 (1985), 93–103.
7. Davy, S.K., Allemand, D., Weis, V.M., Cell biology of cnidarian–dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76 (2012), 229–261.
8. DeSalvo, M.K., Voolstra, C.R., Sunagawa, S., Schwarz, J.A., Stillman, J.H., Coffroth, M.A., Szmant, A.M., Medina, M., Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol. Ecol. 17 (2008), 3952–3971.
9. Detournay, O., Weis, V.M., Role of the sphingosine rheostat in the regulation of cnidarian–dinoflagellate symbioses. Biol. Bull. 221 (2011), 261–269.
10. Douglas, A.E., Coral bleaching – how and why?. Mar. Pollut. Bull. 46 (2003), 385–392.
11. Dubinsky, Z., Coral Reefs. 1990, Elsevier, Amsterdam, New York.
12. Dunn, C.W., Hejnol, A., Matus, D.Q., Pang, K., Browne, W.E., Smith, S.A., Seaver, E., Rouse, G.W., Obst, M., Edgecombe, G.D., Sorensen, M.V., Haddock, S.H.D., Schmidt-Rhaesa, A., Okusu, A., Kristensen, R.M., Wheeler, W.C., Martindale, M.Q., Giribet, G., Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452 (2008), 745–749.
13. Dunn, S.R., Schnitzler, C.E., Weis, V.M., Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: every which way you lose. Proc. R Soc. B 274 (2007), 3079–3085.
14. Dunn, S.R., Thomason, J.C., Le Tissier, M.D., Bythell, J.C., Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration. Cell. Death Differ. 11 (2004), 1213–1222.
15. Fang, F.C., Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat. Rev. Microbiol. 2 (2004), 820–832.
16. Feng, X.H., Derynck, R., Specificity and versatility in TGF-beta signaling through Smads. Annu. Rev. Cell. Dev. Biol. 21 (2005), 659–693.
17. Franchini, A., Malagoli, D., Ottaviani, E., Cytokines and invertebrates: TGF-beta and PDGF. Curr. Pharm. Des. 12 (2006), 3025–3031.
18. Guindon, S., Gascuel, O., A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52 (2003), 696–704.
19. Guindon, S., Lethiec, F., Duroux, P., Gascuel, O., PHYML Online–a web server for fast maximum likelihood-based phylogenetic inference. Nucleic. Acids Res. 33 (2005), W557–W559.
20. Harvell, D., Kim, K., Quirolo, C., Weir, J., Smith, G., Coral bleaching and disease: contributors to 1998 mass mortality in Briareum asbestinum (Octocorallia, Gorgonacea). Hydrobiologia 460 (2001), 97–104.
21. Hausmann, E.H., Hao, S.Y., Pace, J.L., Parmely, M.J., Transforming growth factor beta 1 and gamma interferon provide opposing signals to lipopolysaccharide-activated mouse macrophages. Infect. Immun. 62 (1994), 3625–3632.
22. Hayward, D.C., Samuel, G., Pontynen, P.C., Catmull, J., Saint, R., Miller, D.J., Ball, E.E., Localized expression of a dpp/BMP2/4 ortholog in a coral embryo. Proc. Natl. Acad. Sci. U S A 99 (2002), 8106–8111.
23. Hejnol, A., Obst, M., Stamatakis, A., Ott, M., Rouse, G.W., Edgecombe, G.D., Martinez, P., Bagunà, J., Bailly, X., Jondelius, U., Wiens, M., Müller, W.E.G., Seaver, E., Wheeler, W.C., Martindale, M.Q., Giribet, G., Dunn, C.W., Assessing the root of bilaterian animals with scalable phylogenomic methods. Proceedings of the Royal Society B: Biolog. Sci. 276 (2009), 4261–4270.
24. Heldin, C.H., Miyazono, K., ten Dijke, P., TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390 (1997), 465–471.
25. Hentschel, U., Steinert, M., Hacker, J., Common molecular mechanisms of symbiosis and pathogenesis. Trends Microbiol. 8 (2000), 226–231.
26. Herpin, A., Cunningham, C., Cross-talk between the bone morphogenetic protein pathway and other major signaling pathways results in tightly regulated cell-specific outcomes. FEBS J. 274 (2007), 2977–2985.
27. Herpin, A., Lelong, C., Favrel, P., Transforming growth factor-beta-related proteins: an ancestral and widespread superfamily of cytokines in metazoans. Dev. Comp. Immunol. 28 (2004), 461–485.
28. Hoegh-Guldberg, O., Mumby, P.J., Hooten, A.J., Steneck, R.S., Greenfield, P., Gomez, E., Harvell, C.D., Sale, P.F., Edwards, A.J., Caldeira, K., Knowlton, N., Eakin, C.M., Iglesias-Prieto, R., Muthiga, N., Bradbury, R.H., Dubi, A., Hatziolos, M.E., Coral reefs under rapid climate change and ocean acidification. Sci. 318 (2007), 1737–1742.
29. Jones, R.J., Bowyer, J., Hoegh-Guldberg, O., Blackall, L.L., Dynamics of a temperature-related coral disease outbreak. Mar. Ecol. Prog. Ser. 281 (2004), 63–77.
30. Lehnert, E.M., Burriesci, M.S., Pringle, J.R., Developing the anemone Aiptasia as a tractable model for cnidarian-dinoflagellate symbiosis: the transcriptome of aposymbiotic A. pallida. BMC Genomics, 13, 2012, 271.
31. Lhocine, N., Ribeiro, P.S., Buchon, N., Wepf, A., Wilson, R., Tenev, T., Lemaitre, B., Gstaiger, M., Meier, P., Leulier, F., PIMS modulates immune tolerance by negatively regulating Drosophila innate immune signaling. Cell Host. Microbe. 4 (2008), 147–158.
32. Li, M.O., Wan, Y.Y., Sanjabi, S., Robertson, A.K., Flavell, R.A., Transforming growth factor-beta regulation of immune responses. Annu. Rev. Immunol. 24 (2006), 99–146.
33. Masli, S., Turpie, B., Streilein, J.W., Thrombospondin orchestrates the tolerancepromoting properties of TGF{beta}-treated antigen-presenting cells. Internat Immunol. 18 (2006), 689–699.
34. Massagué, J., TGF-β signal transduction. Annu. Rev. Biochem. 67 (1998), 753–791.
35. Massague, J., Wotton, D., Transcriptional control by the TGF-beta/Smad signaling system. EMBO J. 19 (2000), 1745–1754.
36. Matus, D.Q., Pang, K., Marlow, H., Dunn, C.W., Thomsen, G.H., Martindale, M.Q., Molecular evidence for deep evolutionary roots of bilaterality in animal development. Proc Natl Acad Sci U S A 103 (2006), 11195–11200.
37. Matus, D.Q., Thomsen, G.H., Martindale, M.Q., Dorso/ventral genes are asymmetrically expressed and involved in germ-layer demarcation during cnidarian gastrulation. Curr Biol 16 (2006), 499–505.
38. McFall-Ngai, M., Are biologists in ‘future shock’? Symbiosis integrates biology across domains. Nat. Rev. Microbiol. 6 (2008), 789–792.
39. Nagano, T., Yoshimura, T., Bioimaging of nitric oxide. Chem Rev 102 (2002), 1235–1270.
40. Ndungu, F.M., Urban, B.C., Marsh, K., Langhorne, J., Regulation of immune response by Plasmodium-infected red blood cells. Parasite Immunol 27 (2005), 373–384.
41. Nussler, A.K., Glanemann, M., Schirmeier, A., Liu, L., Nussler, N.C., Fluorometric measurement of nitrite/nitrate by 2,3-diaminonaphthalene. Nature Protoc 1 (2006), 2223–2226.
42. Okamoto, N., McFadden, G.I., The mother of all parasites. Future Microbiol. 3 (2008), 391–395.
43. Padgett, R.W., Wozney, J.M., Gelbart, W.M., Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo. Proc Natl Acad Sci U S A 90 (1993), 2905–2909.
44. Pang, K., Ryan, J.F., Baxevanis, A.D., Martindale, M.Q., Evolution of the TGF-b signaling pathway and its potential role in the Ctenophore, Mnemiopsis leidyi. PLOS One, 6, 2011, e24152.
45. Patel, S.N., Lu, Z., Ayi, K., Serghides, L., Gowda, D.C., Kain, K.C., Disruption of CD36 impairs cytokine response to Plasmodium falciparum glycosylphosphatidylinositol and confers susceptibility to severe and fatal malaria in vivo. J Immunol 178 (2007), 3954–3961.
46. Perez, S., Weis, V.M., Nitric oxide and cnidarian bleaching: an eviction notice mediates breakdown of a symbiosis. J. Exp. Biol. 209 (2006), 2804–2810.
47. Rambaut, A., 2007. FigTree, a graphical viewer of phylogenetic trees. http://tree.bio.ed.ac.uk/software/figtree/.
48. Relman, D.A., ‘Til death do us part’: coming to terms with symbiotic relationships. Forward. Nat. Rev. Microbiol. 6 (2008), 721–724.
49. Ritchie, K.B., Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar. Ecol. Prog. Ser. 322 (2006), 1–14.
50. Rodriguez-Lanetty, M., Harri, S., Hoegh-Guldburg, O., Early molecular responses of coral larvae to hyperthermal stress. Mol. Ecol. 18 (2009), 5101–5114.
51. Rodriguez-Lanetty, M., Phillips, W.S., Weis, V.M., Transcriptome analysis of a cnidarian–dinoflagellate mutualism reveals complex modulation of host gene expression. BMC Genomics, 7, 2006, 23.
52. Ronquist, F., Huelsenbeck, J.P., MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 (2003), 1572–1574.
53. Rosenberg, E., Koren, O., Reshef, L., Efrony, R., Zilber-Rosenberg, I., The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microbiol. 5 (2007), 355–362.
54. Ruscetti, F., Varesio, L., Ochoa, A., Ortaldo, J., Pleiotropic effects of transforming growth factor-beta on cells of the immune system. Ann. N Y Acad. Sci. 685 (1993), 488–500.
55. Saina, M., Technau, U., Characterization of myostatin/gdf8/11 in the starlet sea anemone Nematostella vectensis. J. Exp. Zool. (Mol. Dev. Evol.) 312B (2009), 780–788.
56. Sampath, T.K., Rashka, K.E., Doctor, J.S., Tucker, R.F., Hoffmann, F.M., Drosophila transforming growth factor beta superfamily proteins induce endochondral bone formation in mammals. Proc. Natl. Acad. Sci. U S A 90 (1993), 6004–6008.
57. Samuel, G., Miller, D., Saint, R., Conservation of a DPP/BMP signaling pathway in the nonbilateral cnidarian Acropora millepora. Evol. Dev. 3 (2001), 241–250.
58. Schneider, D.S., Ayres, J.S., Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat. Rev. Immunol. 8 (2008), 889–895.
59. Schwarz, J.A., Understanding the intracellular niche in cnidarian–symbiodinium symbioses: parasites lead the way. Vie Milieu 58 (2008), 141–151.
60. Schwarz, J.A., Brokstein, P.B., Voolstra, C., Terry, A.Y., Manohar, C.F., Miller, D.J., Szmant, A.M., Coffroth, M.A., Medina, M., Coral life history and symbiosis: functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata. BMC Genomics, 9, 2008, 97.
61. Simmons, K.J., Nde, P.N., Kleshchenko, Y.Y., Lima, M.F., Villalta, F., Stable RNA interference of host thrombospondin-1 blocks Trypanosoma cruzi infection. FEBS Lett. 580 (2006), 2365–2370.
62. Srivastava, M., Simakov, O., Chapman, J., Fahey, B., Gauthier, M.E.A., Mitros, T., Richards, G.S., Conaco, C., Dacre, M., Hellsten, U., Larroux, C., Putnam, N.H., Stanke, M., Adamska, M., Darling, A., Degnan, S.M., Oakley, T.H., Plachetzki, D.C., Zhai, Y., Adamski, M., Calcino, A., Cummins, S.F., Goodstein, D.M., Harris, C., Jackson, D.J., Leys, S.P., Shu, S., Woodcroft, B.J., Vervoort, M., Kosik, K.S., Manning, G., Degnan, B.M., Rokhsar, D.S., The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466 (2010), 720–726.
63. Stamatakis, A., RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22 (2006), 2688–2690.
64. Sunagawa, S., Wilson, E., Thaler, M., Smith, M., Caruso, C., Pringle, J., Weis, V., Medina, M., Schwarz, J., Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. BMC Genomics, 10, 2009, 258.
65. Technau, U., Rudd, S., Maxwell, P., Gordon, P.M., Saina, M., Grasso, L.C., Hayward, D.C., Sensen, C.W., Saint, R., Holstein, T.W., Ball, E.E., Miller, D.J., Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. Trends Genet. 21 (2005), 633–639.
66. ten Dijke, P., Miyazono, K., Heldin, C.H., Signaling via hetero-oligomeric complexes of type I and type II serine/threonine kinase receptors. Curr. Opin. Cell Biol. 8 (1996), 139–145.
67. van Oppen, M.J.H., Lough, J.M., Coral Bleaching: Patterns, Processes, Causes and Consequences, Ecological Studies. 2009, Springer, Berlin, Heidelberg.
68. Vidal-Dupiol, J., Adjeroud, M., Roger, E., Foure, L., Duval, D., Mone, Y., Ferrier-Pages, C., Tambutte, E., Tambutte, S., Zoccola, D., Allemand, D., Mitta, G., Coral bleaching under thermal stress: putative involvement of host/symbiont recognition mechanisms. BMC Physicol., 9, 2009, 14.
69. Waghabi, M.C., Keramidas, M., Feige, J.J., Araujo-Jorge, T.C., Bailly, S., Activation of transforming growth factor beta by Trypanosoma cruzi. Cell icrobiol. 7 (2005), 511–517.
70. Weis, V.M., Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J. Exp. Biol. 211 (2008), 3059–3066.
71. Weis, V.M., Davy, S.K., Hoegh-Guldberg, O., Rodriguez-Lanetty, M., Pringle, J.R., Cell biology in model systems as the key to understanding corals. Trends Ecol. Evol. 23 (2008), 369–376.
72. Yang, Y.L., Lin, S.H., Chuang, L.Y., Guh, J.Y., Liao, T.N., Lee, T.C., Chang, W.T., Chang, F.R., Hung, M.Y., Chiang, T.A., Hung, C.Y., CD36 is a novel and potential anti-fibrogenic target in albumin-induced renal proximal tubule fibrosis. J. Cell Biochem. 101 (2007), 735–744.
73. Zoccola, D., Moya, A., Béranger, G., Tambutté, E., Allemand, D., Carle, G., Tambutté, S., Specific expression of BMP2/4 ortholog in biomineralizing tissues of corals and action on mouse BMP receptor. Mar. Biotech. 11 (2009), 260–269.